Modelling the risk of being bitten by malaria vectors in a vector control area in southern Benin, west Africa

Particle and Fibre Toxicology

Hélène Guis³  Vincent Corbel²  Fabrice Chandre¹  Armel Djènontin⁴  Abdul S Bio-Bangana⁴  Nicolas Moiroux¹ 

[1] MIVEGEC (IRD 224-CNRS 5290-UM1-UM2), Institut de Recherche pour le Développement (IRD), BP64501, Montpellier, 34394, France;Department of Entomology, Faculty of Agriculture, Kasetsart University, Bangkok, 10900, Thailand;INRA, UMR 1309 CMAEE, Montpellier, F-34398, France;Centre de Recherche en Entomologie de Cotonou (CREC), Ministère de la Santé, Cotonou, Bénin

关键词: Host-vector contact;    Modelling;    Remote sensing;    Anopheles;    Malaria;   

Others  :  1228032
DOI  :  10.1186/1756-3305-6-71

 received in 2012-10-31, accepted in 2013-03-06,  发布年份 2013

【 摘 要 】

Background

The diversity of malaria vector populations, expressing various resistance and/or behavioural patterns could explain the reduced effectiveness of vector control interventions reported in some African countries. A better understanding of the ecology and distribution of malaria vectors is essential to design more effective and sustainable strategies for malaria control and elimination. Here, we analyzed the spatio-temporal risk of the contact between humans and the sympatric An. funestus and both M and S molecular forms of An. gambiae s.s. in an area of Benin with high coverage of vector control measures with an unprecedented level of resolution.

Methods

Presence-absence data for the three vectors from 1-year human-landing collections in 19 villages were assessed using binomial mixed-effects models according to vector control measures and environmental covariates derived from field and remote sensing data. After 8-fold cross-validations of the models, predictive maps of the risk of the contact between humans and the sympatric An. funestus and both molecular M and S forms of An. gambiae s.s. were computed.

Results

Model validations showed that the An. funestus, An. gambiae M form, and S form models provided an excellent (Area Under Curve>0.9), a good (AUC>0.8), and an acceptable (AUC>0.7) level of prediction, respectively. The distribution area of the probability of contact between human and An. funestus largely overlaps that of An. gambiae M form but this latter showed important seasonal variation. An. gambiae S form also showed seasonal variation but with different ecological preferences. Landscape data were useful to discriminate between the species’ distributions.

Conclusions

These results showed that available remote sensing data could help in predicting the human-vector contact for several species of malaria vectors at a village level scale. The predictive maps showed seasonal and spatial variations in the risk of human-vector contact for all three vectors. Such maps could help Malaria Control Programmes to implement more effective vector control strategy by taking into account to the dynamics of malaria vector species.

【 授权许可】

   
2013 Moiroux et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD: Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012, 379:413-431.
• [2]World Health Organization: World Malaria Report 2011. Geneva: World Health Organization; 2011:259.
• [3]Feachem R, Sabot O: A new global malaria eradication strategy. Lancet 2008, 371:1633-1635.
• [4]Trape JF, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, Dieye-Ba F, Roucher C, Bouganali C, Badiane A: Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet Infect Dis 2011, 11:925-932.
• [5]Corbel V, Akogbeto M, Damien GB, Djenontin A, Chandre F, Rogier C, Moiroux N, Chabi J, Banganna B, Padonou GG, Henry MC: Combination of malaria vector control interventions in pyrethroid resistance area in Benin: a cluster randomised controlled trial. Lancet Infect Dis 2012, 12:617-626.
• [6]Asidi A, N'Guessan R, Akogbeto M, Curtis C, Rowland M: Loss of household protection from use of insecticide-treated nets against pyrethroid-resistant mosquitoes, benin. Emerg Infect Dis 2012, 18:1101-1106.
• [7]Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, Gimnig JE, Fish D, Killeen GF: Ecology: a prerequisite for malaria elimination and eradication. PLoS Med 2010, 7:e1000303.
• [8]The malERA Consultative Group on Vector Control: A Research Agenda for Malaria Eradication: Vector Control. PLoS Med 2011, 8:e1000401.
• [9]Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T, Coetzee M, Mbogo CM, Hemingway J, Patil AP, Temperley WH: A global map of dominant malaria vectors. Parasit Vectors 2012, 5:69. BioMed Central Full Text
• [10]Manguin S, Carnevale P, Mouchet J, Coosemans M, Julvez J, Richard-Lenoble D, Sircoulon J: Biodiversity of malaria in the world. Montrouge, France: John Libbey Eurotext; 2008.
• [11]Cohuet A, Harris C, Robert V, Fontenille D: Evolutionary forces on Anopheles: what makes a malaria vector. Trends Parasitol 2010, 26:130-136.
• [12]Della Torre A, Tu Z, Petrarca V: On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. Insect Biochem Mol Biol 2005, 35:755-769.
• [13]Simard F, Ayala D, Kamdem GC, Pombi M, Etouna J, Ose K, Fotsing JM, Fontenille D, Besansky NJ, Costantini C: Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecol 2009, 9:17. BioMed Central Full Text
• [14]Costantini C, Ayala D, Guelbeogo WM, Pombi M, Some CY, Bassole IH, Ose K, Fotsing JM, Sagnon N, Fontenille D: Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecol 2009, 9:16. BioMed Central Full Text
• [15]Kelly-Hope L, Lawson B, Wilson M, Boakye D, De Souza D: Environmental factors associated with the distribution of Anopheles gambiae s.s in Ghana; an important vector of lymphatic filariasis and malaria. PLoS One 2010, 5:e9927.
• [16]Ndiath MO, Cohuet A, Gaye A, Konate L, Mazenot C, Faye O, Boudin C, Sokhna C, Trape JF: Comparative susceptibility to Plasmodium falciparum of the molecular forms M and S of Anopheles gambiae and Anopheles arabiensis. Malar J 2011, 10:269. BioMed Central Full Text
• [17]Gimonneau G, Pombi M, Choisy M, Morand S, Dabire RK, Simard F: Larval habitat segregation between the molecular forms of the mosquito Anopheles gambiae in a rice field area of Burkina Faso, West Africa. Med Vet Entomol 2011, 26:9-17.
• [18]Diabate A, Dabire RK, Heidenberger K, Crawford J, Lamp WO, Culler LE, Lehmann T: Evidence for divergent selection between the molecular forms of Anopheles gambiae: role of predation. BMC Evol Biol 2008, 8:5. BioMed Central Full Text
• [19]Diabate A, Dabire RK, Kim EH, Dalton R, Millogo N, Baldet T, Simard F, Gimnig JE, Hawley WA, Lehmann T: Larval development of the molecular forms of Anopheles gambiae (Diptera: Culicidae) in different habitats: a transplantation experiment. J Med Entomol 2005, 42:548-553.
• [20]Gimonneau G, Bouyer J, Morand S, Besansky NJ, Diabate A, Simard F: A behavioral mechanism underlying ecological divergence in the malaria mosquito Anopheles gambiae. Behav Ecol 2010, 21:1087-1092.
• [21]Gimonneau G, Pombi M, Dabire RK, Diabate A, Morand S, Simard F: Behavioural responses of Anopheles gambiae sensu stricto M and S molecular form larvae to an aquatic predator in Burkina Faso. Parasit Vectors 2012, 5:65. BioMed Central Full Text
• [22]Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V: Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 2011, 27:91-98.
• [23]Moiroux N, Gomez MB, Pennetier C, Elanga E, Djenontin A, Chandre F, Djegbe I, Guis H, Corbel V: Changes in Anopheles funestus Biting Behavior Following Universal Coverage of Long-Lasting Insecticidal Nets in Benin. J Infect Dis 2012, 206:1622-1629.
• [24]Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF: Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J 2011, 10:80. BioMed Central Full Text
• [25]Govella NJ, Ferguson H: Why Use of Interventions Targeting Outdoor Biting Mosquitoes will be Necessary to Achieve Malaria Elimination. Front Physiol 2012, 3:199.
• [26]Diabate A, Baldet T, Chandre C, Dabire KR, Kengne P, Guiguemde TR, Simard F, Guillet P, Hemingway J, Hougard JM: KDR mutation, a genetic marker to assess events of introgression between the molecular M and S forms of Anopheles gambiae (Diptera: Culicidae) in the tropical savannah area of West Africa. J Med Entomol 2003, 40:195-198.
• [27]Chandre F, Manguin S, Brengues C, Dossou Yovo J, Darriet F, Diabate A, Carnevale P, Guillet P: Current distribution of a pyrethroid resistance gene (kdr) in Anopheles gambiae complex from west Africa and further evidence for reproductive isolation of the Mopti form. Parassitologia 1999, 41:319-322.
• [28]Fanello C, Petrarca V, Della Torre A, Santolamazza F, Dolo G, Coulibaly M, Alloueche A, Curtis CF, Toure YT, Coluzzi M: The pyrethroid knock-down resistance gene in the Anopheles gambiae complex in Mali and further indication of incipient speciation within An. gambiae s.s. Insect Mol Biol 2003, 12:241-245.
• [29]Santolamazza F, Calzetta M, Etang J, Barrese E, Dia I, Caccone A, Donnelly MJ, Petrarca V, Simard F, Pinto J, Della Torre A: Distribution of knock-down resistance mutations in Anopheles gambiae molecular forms in west and west-central Africa. Malar J 2008, 7:74. BioMed Central Full Text
• [30]Dabire KR, Diabate A, Djogbenou L, Ouari A, N'Guessan R, Ouedraogo JB, Hougard JM, Chandre F, Baldet T: Dynamics of multiple insecticide resistance in the malaria vector Anopheles gambiae in a rice growing area in South-Western Burkina Faso. Malar J 2008, 7:188. BioMed Central Full Text
• [31]Djenontin A, Bio-Bangana S, Moiroux N, Henry MC, Bousari O, Chabi J, Osse R, Koudenoukpo S, Corbel V, Akogbeto M, Chandre F: Culicidae diversity, malaria transmission and insecticide resistance alleles in malaria vectors in Ouidah-Kpomasse-Tori district from Benin (West Africa): A pre-intervention study. Parasit Vectors 2010, 3:83. BioMed Central Full Text
• [32]Brooke BD, Kloke G, Hunt RH, Koekemoer LL, Temu EA, Taylor ME, Small G, Hemingway J, Coetzee M: Bioassay and biochemical analyses of insecticide resistance in southern African Anopheles funestus (Diptera: Culicidae). Bull Entomol Res 2001, 91:265-272.
• [33]Dabire RK, Namountougou M, Sawadogo SP, Yaro LB, Toe HK, Ouari A, Gouagna LC, Simard F, Chandre F, Baldet T: Population dynamics of Anopheles gambiae s.l. in Bobo-Dioulasso city: bionomics, infection rate and susceptibility to insecticides. Parasit Vectors 2012, 5:127. BioMed Central Full Text
• [34]Corbel V, N'Guessan R, Brengues C, Chandre F, Djogbenou L, Martin T, Akogbeto M, Hougard JM, Rowland M: Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop 2007, 101:207-216.
• [35]Djogbenou L, Pasteur N, Akogbeto M, Weill M, Chandre F: Insecticide resistance in the Anopheles gambiae complex in Benin: a nationwide survey. Med Vet Entomol 2011, 25:256-267.
• [36]Djegbe I, Boussari O, Sidick A, Martin T, Ranson H, Chandre F, Akogbeto M, Corbel V: Dynamics of insecticide resistance in malaria vectors in Benin: first evidence of the presence of L1014S kdr mutation in Anopheles gambiae from West Africa. Malar J 2011, 10:261. BioMed Central Full Text
• [37]Gillies M, Coetzee M: A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical Region). Johannesburg, South Africa: South African Institute for Medical Research; 1987.
• [38]Gillies M, De Meillon B: The Anophelinae of Africa South of the Sahara (Ethiopian Zoogeographical Region). Publication of the South Afr Inst Med Res 1968, 54:1-343.
• [39]Koekemoer LL, Kamau L, Hunt RH, Coetzee M: A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. AmJTrop Med Hyg 2002, 66:804-811.
• [40]Scott JA, Brogdon WG, Collins FH: Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. AmJTrop Med Hyg 1993, 49:520-529.
• [41]Favia G, Lanfrancotti A, Spanos L, Siden-Kiamos I, Louis C: Molecular characterization of ribosomal DNA polymorphisms discriminating among chromosomal forms of Anopheles gambiae s.s. Insect Mol Biol 2001, 10:19-23.
• [42]Silver JB: Sampling the Larval Population. Ecology: In Mosquito; 2008:137-338.
• [43]World Health Organization: Yellow-fever panel: report on the first session. Geneva: World Health Organization; 1950:12.
• [44]Service MW: Mosquito (Diptera: Culicidae) dispersal–the long and short of it. J Med Entomol 1997, 34:579-588.
• [45]Colditz RR, Conrad C, Wehrmann T, Schmidt M, Dech S: TiSeG: A flexible software tool for time-series generation of MODIS data utilizing the quality assessment science data set. IEEE Trans Geosci Remote Sens 2008, 46:3296-3308.
• [46]Volkoff B, Willaime P: Carte pédologique de reconnaissance de la République Populaire du Bénin à 1/200 000: feuille de Porto-Novo. Paris: ORSTOM; 1976:41.
• [47]Aubert G: La classification pédologique utilisée en France. In Classification des Sols. Gand: Symposium International; 1965:25-56.
• [48]Young A: Tropical soils and soil survey. Cambridge: Cambridge Univ. Press; 1976.
• [49]Benz UC, Hofmann P, Willhauck G, Lingenfelder I, Heynen M: Multi-resolution, object-oriented fuzzy analysis of remote sensing data for GIS-ready information. ISPRS J Photogramm Remote Sens 2004, 58:239-258.
• [50]McGarigal K, Cushman S, Ene E: FRAGSTATS v4: Spatial Pattern Analysis Program for Categorical and Continuous Maps. In Book FRAGSTATS v4: Spatial Pattern Analysis Program for Categorical and Continuous Maps. City: University of Massachusetts; 2012.
• [51]Killeen GF, Smith TA: Exploring the contributions of bed nets, cattle, insecticides and excitorepellency to malaria control: a deterministic model of mosquito host-seeking behaviour and mortality. Trans R Soc Trop Med Hyg 2007, 101:867-880.
• [52]R Development Core Team: R: A Language and Environment for Statistical Computing. Austria: R Foundation for Statistical Computing; 2010.
• [53]Bates D, Maechler M: lme4: Linear mixed-effects models using S4 classes. 2009. R package version 0.999375-32
• [54]Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, Muller M: pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinforma 2011, 12:77. BioMed Central Full Text
• [55]Zuur AF, Ieno EN, Elphick CS: A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 2010, 1:3-14.
• [56]Park SH, Goo JM, Jo CH: Receiver operating characteristic (ROC) curve: practical review for radiologists. Korean J Radiol 2004, 5:11-18.
• [57]Djogbenou L, Pasteur N, Bio-Bangana S, Baldet T, Irish SR, Akogbeto M, Weill M, Chandre F: Malaria vectors in the Republic of Benin: Distribution of species and molecular forms of the Anopheles gambiae complex. Acta Trop 2010, 114:116-122.
• [58]Hamon J: Biologie d'Anopheles funestus. In Biologie des anophèles d'AOF et d'AEF. Paris: ORSTOM; 1955:6.
• [59]Edillo FE, Toure YT, Lanzaro GC, Dolo G, Taylor CE: Spatial and habitat distribution of Anopheles gambiae and Anopheles arabiensis (Diptera: Culicidae) in Banambani village, Mali. J Med Entomol 2002, 39:70-77.
• [60]Anosike JC, Nwoke BE, Okere AN, Oku EE, Asor JE, Emmy-Egbe IO, Adimike DA: Epidemiology of tree-hole breeding mosquitoes in the tropical rainforest of Imo State, south-east Nigeria. Ann Agric Environ Med 2007, 14:31-38.
• [61]Bayoh MN, Lindsay SW: Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (Diptera: Culicidae). Bull Entomol Res 2003, 93:375-381.
• [62]Bayoh MN, Lindsay SW: Temperature-related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory. Med Vet Entomol 2004, 18:174-179.
• [63]Lyimo EO, Takken W, Koella JC: Effect of rearing temperature and larval density on larval survival, age at pupation and adult size of Anopheles gambiae. Entomol Exp Appl 1992, 63:265-271.
• [64]Moiroux N, Boussari O, Djènontin A, Damien G, Cottrell G, Henry M-C, Guis H, Corbel V: Dry Season Determinants of Malaria Disease and Net Use in Benin. West Africa. PLoS One 2012, 7:e30558.
• [65]White MT, Griffin JT, Churcher TS, Ferguson NM, Basanez MG, Ghani AC: Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasit Vectors 2011, 4:153. BioMed Central Full Text
• [66]Lines JD, Myamba J, Curtis CF: Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Med Vet Entomol 1987, 1:37-51.
• [67]Fillinger U, Lindsay SW: Larval source management for malaria control in Africa: myths and reality. Malar J 2011, 10:353. BioMed Central Full Text
• [68]Worrall E, Fillinger U: Large-scale use of mosquito larval source management for malaria control in Africa: a cost analysis. Malar J 2011, 10:338. BioMed Central Full Text